Cytosolic HSP90 Regulates the Heat Shock Response That Is Responsible for Heat Acclimation in Arabidopsis thaliana

Abstract

Plant survival requires the ability to acclimate to heat. When plants are subjected to heat shock, the expression of various genes is induced, and the plants become tolerant of higher temperatures. We found that transient treatment with geldanamycin and radicicol, two heat shock protein 90 (HSP90) inhibitors, induced heat-inducible genes and heat acclimation in Arabidopsis thaliana seedlings. Heat shock reduced the activity of exogenously expressed glucocorticoid receptor (GR). Since GR activity depends on HSP90, this suggests that heat shock reduces cytosolic HSP90 activity in vivo. Microarray analysis revealed that many of the genes that are up-regulated by both heat shock and HSP90 inhibitors are involved in protein folding and degradation, suggesting that the activation of a protein maintenance system is a crucial part of this response. Most of these genes have heat shock response element-like motifs in their promoters, which suggests that heat shock transcription factor (HSF) is involved in the response to HSP90 inhibition. Several HSF genes are expressed constitutively in A. thaliana, including AtHsfA1d. Recombinant AtHsfA1d protein recognizes the heat shock response element motif and interacts with A. thaliana cytosolic HSP90, HSP90.2. Overexpression of a dominant negative form of HSP90.2 induced the heat-inducible gene. Thus, it appears that in the absence of heat shock, cytosolic HSP90 negatively regulates heat-inducible genes by actively suppressing HSF function. Upon heat shock, cytosolic HSP90 is transiently inactivated, which may lead to HSF activation.

OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.)

“…It may be inferred that HS-induced OsHsfA2c binds to OsClpB-cyt promoter, possibly controlling synthesis of the OsClpB-cyt transcript. We suggest that the binding of OsClpB-cyt with OsHsfA2c may work in a negative feedback loop manner as reported for Hsp90 (Yamada et al 2007). Interactions between HSPs and HSFs have been documented previously.…”

“…Cytosolic Hsp90 in Arabidopsis interacts with constitutively expressed HsfA4 to down-regulate its function. Detailed analysis further reflected that Hsp90.2 interacts with AtHsfA7a and AtHsfB1 and not with AtHsfA4c (Yamada et al 2007;Yamada and Nishimura 2008).…”

Generation of transgenic rice expressing heat shock protein genes under cool conditions

“…When the seedlings of WCR::Hsf transformants were treated with 50 µM geldanamycin (GDM), an inhibitor of HSP90, the expression levels of sHSPs were higher than those of the non-transformant. These results strongly suggested that induction of the heat shock response in rice is controlled by HSP90 activity (Yamada et al 2007). Therefore, we generated transgenic rice overexpressing Hsfs in a dominant negative HSP90 mutant.…”

Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response

“…[5][6][7] For many years, the activation of HSPs following a sharp temperature increase was thought to be regulated by denatured cytosolic proteins, that upon sequestering Hsp70 and Hsp90, would derepress heat shock transcription factors (HSFs), thereby inducing the upregulation of heat shock genes. [8][9][10] Yet, the overexpression of HSPs, so called the heat shock response (HSR), can be activated under mild physiological conditions that are unlikely to cause any protein denaturation in the cell. [11][12][13] Although multiple HSR triggering mechanisms may co-exist, 6,[14][15][16] recent evidences in bacteria, algae, plants and mammalian cells point at the understanding how plants sense and respond to heat stress is central to improve crop tolerance and productivity.…”